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Transcript
Evaluation of fluorodeoxyglucose positron
emission tomography in the management of
soft-tissue sarcomas
J. D. Lucas, M. J. O’Doherty, J. C. H. Wong, J. B. Bingham,
P. H. McKee, C. D. M. Fletcher, M. A. Smith
From St Thomas’ Hospital, London, England
e performed a retrospective analysis to evaluate
18
the ability of whole-body F-fluorodeoxyglucose
positron emission tomography (FDG PET) to identify
local recurrence and pulmonary metastases in patients
with soft-tissue tumours after treatment. We compared
the results of FDG PET with those of MRI for the
detection of local recurrence, and with CT of the chest
for pulmonary metastases.
We assessed 62 patients of mean age 51 years, who
had 15 types of soft-tissue sarcoma, after a mean
follow-up of 3 years 2 months. For the detection of
local disease, 71 comparisons showed that the
sensitivity and specificity of FDG PET were 73.7%
and 94.3%, respectively; there were 14 true-positive
and five false-negative results. MRI had a sensitivity
and specificity of 88.2% and 96.0% respectively. For
the identification of lung metastases, 70 comparisons
showed that the sensitivity and specificity of FDG PET
were 86.7% and 100%, with 13 true-positive results
and two false-negative results. CT of the chest had a
sensitivity and specificity of 100% and 96.4%.
Thirteen other sites of metastases were identified by
FDG PET.
FDG PET can identify both local and distant
recurrence of tumour as a one-step procedure and
will detect other metastases. It seems that all three
methods of imaging are needed to define accurately
W
J. D. Lucas, FRCS, Clinical Lecturer in Orthopaedics
M. A. Smith, FRCS, Consultant Orthopaedic Surgeon
M. J. O’Doherty, FRCP, Senior Lecturer in Radiological Sciences and
Honorary Consultant Physician
P. H. McKee, FRCPath, Senior Lecturer and Honorary Consultant in
Histopathology
J. B. Bingham, FRCP, FRCR
UMDS and Guy’s and St Thomas’ Hospital Trust, St Thomas’ Hospital,
Lambeth Palace Road, London SE1 7EH, UK.
C. D. M. Fletcher, FRCPath, Professor and Director of Surgical
Pathology
Brigham and Women’s Hospital, Boston, Massachusetts 02115, USA.
J. C. H. Wong, FRACP, Consultant Physician and Clinical Senior
Lecturer
Royal Brisbane Hospital, Herston, Queensland 4029, Australia.
Correspondence should be sent to Mr M. A. Smith.
©1998 British Editorial Society of Bone and Joint Surgery
0301-620X/98/38232 $2.00
VOL. 80-B, NO. 3, MAY 1998
the extent of disease, both at initial staging and
during follow-up.
J Bone Joint Surg [Br] 1998;80-B:441-7.
Received 31 July 1997; Accepted 24 September 1997
Adult soft-tissue sarcomas (STS) are a heterogeneous
group of rare malignant tumours arising from soft tissues
and account for approximately 1% of all cancers. The
incidence in England and Wales is 1.7 per 100 000 men and
1.4 per 100 000 women giving approximately 1000 to 1500
1
new cases per year. In the USA, there are approximately
2
7000 new cases per year. When first seen, between 10%
and 23% of patients will have metastases, the lung being
the most common site with one-third of secondary tumours.
Deposits in bone, liver, and brain comprise about 40%; the
others are found in the regional lymph nodes, retroper3,4
itoneum and soft tissues.
After treatment of the primary tumour between 30% and
35% of patients will develop recurrence either locally or at
5,6
a distant site. Of these patients, between 15% and 47%
will develop a local recurrence, depending on the margins
achieved at surgical resection. Isolated metastases are seen
in the lung in 38% to 64%, and from 28% to 34% will
5-7
develop metastases at multiple sites.
The optimal management of these tumours depends on
the site, size and grade of the local growth and accurate
staging of the disease when first seen. The site and size are
8-10
best determined by MRI,
but the accurate diagnosis of
distant metastases is confounded by the wide distribution of
potential sites. The detection of local recurrence is hampered by difficulty in differentiating between recurrence,
the changes after operation, and the effect of any
radiotherapy.
Local recurrence is best assessed using MRI with gadolinium contrast enhancement; regular clinical examination
alone is insensitive. MRI has a sensitivity of 80% to 85%
for the detection of local recurrence, better than CT which
11-14
Ultrasound has a
has a sensitivity of 57% to 70%.
similar sensitivity to MRI for the detection of local recurrence, but depends very much on the proficiency of the
10,12
operator.
A variety of radionucleide methods has been
14,15
tried with varying success.
Lung metastases can be identified using CT, but other
441
442
J. D. LUCAS,
M. J. O’DOHERTY,
potential sites of metastases need to be specifically examined. Whole-body gallium scanning has been used to identify sites of metastases to aid in the staging at presentation
and after treatment; it provides sensitivities of from 72% to
15-19
93%.
There is concern about the ability to detect
subclinical recurrences.
18
F-fluorodeoxyglucose positron emission tomography
(FDG PET) can successfully identify primary, recurrent and
metastatic cancer of the breast, colon, lung and the lympho20
mas. It can detect STS and give an indication of
21-25
There is limited information on its use in the
grade.
early detection of local recurrence and metastases after
primary surgical treatment of STS. FDG PET has the
potential advantage of identifying both complications by a
single procedure, and we have tried to evaluate this.
Patients and Methods
The 62 patients whom we studied had an STS treated
between April 1988 and November 1995. The 34 men and
28 women had a mean age, at the time of diagnosis, of 50
years 11 months (2 years 11 months to 83 years 8 months).
The mean follow-up from the time of accurate diagnosis,
when operation had provided a definitive histological diagnosis, to the latest examination or death was 3 years 2
months (1 month to 9 years 1 month). The minimum
follow-up was of a patient with a high-grade leiomyosarcoma with pulmonary metastases, who left the country to seek
medical advice elsewhere.
Routine follow-up had been by traditional imaging techniques and, since 1992, also by whole-body FDG PET. We
reviewed all FDG PET scans in a blinded manner with no
reference to other imaging (MJO’D, JCHW). Two patients
had whole-body FDG PET when first seen as part of the
evaluation for staging, and were therefore only included in
the assessment of the value of FDG PET in detecting
distant metastases. We compared FDG PET findings with
those of clinical examination, MRI and CT for local recurrence, and with histology when a biopsy had been performed. For the assessment of the detection of lung
metastases, FDG PET was compared with CT of the chest,
and with histological examination when available. Scans
for other sites of metastases were evaluated against clinical
examination, other imaging techniques as indicated, and the
histology of biopsy material. Our absolute standard for the
diagnosis of tumour recurrence both locally and at distant
sites was histological examination. We tried to minimise
the risk of false-negative results by maintaining a low
threshold for biopsy material and by additional imaging.
Histology. The histological diagnosis and grading of the
primary tumours were by two histopathologists (CDMF
and PHM). Tumour differentiation, necrosis and the mitotic
count were assessed to determine whether the tumour was
26,27
grade 1, low; grade 2, intermediate; or grade 3, high.
The FDG PET scan. All patients had standard whole-body
scanning after a six-hour fast. An emission whole-body
J. C. H. WONG,
ET AL
scan was performed after the intravenous injection of
350 MBq FDG using an ECAT 951R Whole Body System
(Siemens/CTI, Knoxville, Tennessee) with an image resolution of 8 mm and an axial field of view of 10.6 cm. The
images were displayed as coronal, sagittal and transaxial
sections. Areas with abnormally increased FDG uptake
were noted and a decision made as to whether or not this
represented potential malignant disease. Focal areas of
uptake with activity equal to, or greater than, liver uptake
were scored as metastatic. When the changes were at the
site of recent surgery, a decision was made between reactive change and malignant disease.
MRI of the local site. Axial T1-weighted images with
coronal STIR were followed by post-contrast axial T1
images with fat suppression. Gadolinium diethylenetriamine penta-acetic acid was given intravenously at a dose of
0.2 ml/kg of body-weight. The proximal and distal ends of
the surgical scar were marked with oil capsules. All scans
were reviewed blind and independently by an MR radiologist (JBB).
CT of the chest. Before May 1996 we used an 8 mm on
8 mm post-contrast scan using a Siemens CT scanner.
Ultravist 370 (Schering Health Care Ltd, Burgess Hill, UK)
was used as the contrast medium with 100 ml administered
intravenously by hand; scanning started after 50 ml had
been infused. From May 1996 a 10 mm on 10 mm volume
spiral post-contrast scan was performed using a Philips
Tomoscan AV/Spiral. Ultravist 370 was given intravenously
with 75 ml injected at a rate of 3 ml/min, the scan starting
ten seconds after infusion had commenced. Contrast administration and the scan start time were automated. All scans
were reviewed blind and independently by one author
(JBB).
Results
There were 15 types of sarcoma, liposarcoma being the
most common (Table I). They were in 13 different sites, the
Table I. Histological types and frequency of the 15 STS
Number of
patients
Sarcoma type
Liposarcoma
Synovial sarcoma
Leiomyosarcoma
Myxofibrosarcoma (myxoid MFH)*
Unclassifiable pleomorphic sarcoma
Extraskeletal osteosarcoma
Malignant peripheral nerve sheath tumour (MPNST)
Round-cell sarcoma
Angiomatoid MFH
Epithelioid angiosarcoma
Clear-cell sarcoma (malignant melanoma of soft parts)
Alveolar rhabdomyosarcoma
Epithelioid sarcoma
Fibromyxoid sarcoma
Triton sarcoma (MPNST with rhabdomyoplastic
differentiation)
18
12
9
5
4
3
2
2
1
1
1
1
1
1
1
Total
62
* malignant fibrous histiocytoma
THE JOURNAL OF BONE AND JOINT SURGERY
FLUORODEOXYGLUCOSE POSITRON EMISSION TOMOGRAPHY IN SOFT-TISSUE SARCOMAS
Table II. Sites and frequency
of the 15 STS
Site
Number of
patients
Trunk
Shoulder girdle
Arm
Elbow
Forearm
Hand
Groin
Buttock
Thigh
Knee
Leg
Ankle
Foot
3
5
1
4
1
2
1
3
25
5
6
4
2
Total
62
Table III. The grades and frequency of the STS according to the
26
system of Trojani
Sarcoma grade
Number of
patients
High
Intermediate
Low
47
7
8
Total
62
commonest being the thigh (Table II). The distribution of
the grades of the tumours is shown in Table III.
Detection of local recurrence. In the group of 60 patients
available for assessment, there were 72 comparisons of
FDG PET with MRI in 67, CT in four and clinical examination alone in one patient who was subsequently shown
443
to have a recurrence on histological examination. Biopsies
were performed when changes on the scans suggested a
recurrence. The median time between FDG PET and MRI
or CT was one day (1 to 63).
FDG PET showed a sensitivity of 73.7% with a specificity of 94.3%. There were five false-negative results in
each of which a recurrence was proven on histological
examination. MRI had also been undertaken in four of
these and had failed to identify the recurrence in two; in the
fifth, false-negative CT had failed to diagnose the recurrence (Table IV). One false-negative result was for an
intermediate-grade myxofibrosarcoma at the ankle, two
were liposarcomas in the thigh (one high-grade round-cell
and one an intermediate atypical dedifferentiated liposarcoma), one was an alveolar rhabdomyosarcoma in the thigh,
and one was a synovial sarcoma at the knee. MRI failed to
identify local recurrence of the high-grade liposarcoma and
of the alveolar rhabdomyosarcoma, and CT did not show
the recurrence of the synovial sarcoma.
FDG PET gave three-false positive results. These were
for a high-grade clear-cell sarcoma (malignant melanoma
of soft parts) in the foot, and two low-grade myxoid
liposarcomas in the thigh. MRI gave false-positive results
for the clear-cell sarcoma and one of the liposarcomas. All
three patients had incisional biopsies under general anaesthesia to provide multiple tissue samples which showed no
recurrence of tumour.
MRI had a sensitivity of 88.2% with a specificity of
96.0% (Table IV). Of the 15 incidences of local recurrence
detected (Fig. 1), all were confirmed histologically; only
two of them had been identified on clinical examination.
Patients with negative FDG PET were followed subse-
Table IV. Results for the detection of local recurrence
Investigation
True-negative
False-negative
True-positive
False-positive
Total
Sensitivity
(%)
Specificity
(%)
FDG PET
MRI
50
48
5
2
14
15
3
2
72
67
73.7
88.2
94.3
96.0
Fig. 1a
Fig. 1b
Fig. 1c
Fig. 1d
Recurrence of a synovial sarcoma 2 years and 7 months after the original excision from the posterolateral aspect of the left knee. Figures 1a-c – FDG
PET showed intense uptake posterolateral to the knee (arrows). Figure 1d – T1-weighted post-contrast MRI showed a well-defined area of enhancing
tissue representing recurrence of the tumour (arrow).
VOL. 80-B, NO. 3, MAY 1998
444
J. D. LUCAS,
M. J. O’DOHERTY,
J. C. H. WONG,
ET AL
Table V. Results for the detection of lung metastases
Investigation
True-negative
False-negative
True-positive
False-positive
Total
Sensitivity
(%)
Specificity
(%)
FDG PET
CT chest
55
53
2
0
13
15
0
2
70
70
86.7
100.0
100.0
96.4
Fig. 2a
Fig. 2b
A high-grade leiomyosarcoma in the thigh which was false-negative for lung metastases.
Figure 2a – FDG PET showing no abnormal uptake in either lung. There is delayed
excretion from the left kidney (arrow) and accumulation of FDG in the bladder. Figure 2b
– CT of the chest showing a large parenchymal lung metastasis (large arrow) and bilateral
changes due to lung atelectasis (small arrows).
quently with further imaging using either FDG PET or
MRI, in combination with clinical examination to determine that no recurrence had occurred.
Detection of lung metastases. In the 62 patients, there were
70 comparisons of FDG PET with CT of the chest and,
when available, tissue diagnosis. FDG PET had a sensitivity
of 86.7% and a specificity of 100%. CT of the chest had a
sensitivity of 100% and a specificity of 96.4% (Table V).
There were two false-negative FDG PET scans in
patients with multiple lung metastases, one from a highgrade extraskeletal osteosarcoma and the other from a highgrade leiomyosarcoma. Tissue diagnosis was not obtained
in either case because the CT findings were considered to
be conclusive (Fig. 2).
THE JOURNAL OF BONE AND JOINT SURGERY
FLUORODEOXYGLUCOSE POSITRON EMISSION TOMOGRAPHY IN SOFT-TISSUE SARCOMAS
445
Table VI. Details of nine patients with metastases at sites other than the lungs
Case
Tumour type
1
2
3
4
Synovial sarcoma
Leiomyosarcoma
Leiomyosarcoma
Epithelioid angiosarcoma
5
6
7
8
9
Round-cell sarcoma
Liposarcoma
Leiomyosarcoma
Leiomyosarcoma
Synovial sarcoma
Sites of metastases
other than lung
Presence of
lung metastases
Tissue diagnosis
of metastases
other than lung
Outcome
Liver, ribs, left adrenal gland
Retroperitoneum
Regional lymph node
Regional lymph node
Subcutaneous, thigh
Subcutaneous, thigh
Thoracic spine
Retroperitoneum
Paraspinal
Subcutaneous, arm
Anterior chest wall
Yes
Yes
Yes
No
No
Yes
Yes
Yes
Died
Died
Died
Alive
Yes
No
Yes
Yes
Yes
Yes
Yes
No
Yes
No
Died
Died
Lost to follow-up
Alive
Died
Fig. 3
Coronal FDG PET scans showing multiple metastases in lung, liver and the left adrenal gland.
There were two false-positive CT scans; the FDG PET
was negative in both. The first was in a patient with a lowgrade fibromyxoid sarcoma in the thigh in whom CT of the
chest showed hilar lymphadenopathy and some nodules
within the lung parenchyma. Two subsequent CT scans
over a period of a year demonstrated resolution of the hilar
lymphadenopathy, but the parenchymal nodules were
unchanged and the patient remains well. The initial diagnosis of metastases was therefore considered to be incorrect. In the second patient, CT showed two distinct masses,
one in the left lower lobe and the other in the right apex,
both of which were thought to be metastases. FDG PET at
the same time showed minor uptake in the left lower zone
only, which was not considered to be significant. Biopsy of
one of the lesions showed it to be a lung infarct.
Detection of sites of metastases other than the lungs. In
nine patients, FDG PET identified 13 sites of metastases
other than in the lungs; seven of them had concurrent lung
metastases (Fig. 3). In eight patients, the sites of the metastases were not clinically evident, and were confirmed by
histological examination (Table VI). At five sites the nature
of the lesion was not confirmed histologically. Three were in
one patient who died from the sarcoma, one was in a patient
VOL. 80-B, NO. 3, MAY 1998
who had an obvious retroperitoneal metastasis confirmed on
CT, and in the other there was an obvious metastasis in the
anterior chest wall which was also seen on CT.
One false-positive FDG PET scan was in a patient who
had had an above-elbow amputation for a high-grade leiomyosarcoma. FDG PET identified a region of intense
uptake in the ipsilateral acromioclavicular joint and in the
subacromial space, which was thought to be a metastasis.
MRI using gadolinium contrast medium showed degenerative changes within the acromioclavicular joint and rotator
cuff, but no evidence of a mass. In another patient with a
synovial sarcoma of the leg, FDG PET identified significant, symmetrical upper hilar lymphadenopathy which
was confirmed by CT. This was not typical of a metastatic
synovial sarcoma and a biopsy was therefore performed
which revealed a grade-two nodular sclerosing Hodgkin’s
lymphoma. This has been classified as a true-negative
result.
Discussion
The behaviour of the lesions in this group of patients is
3-7
representative of the natural history of STS. Of the 60
446
J. D. LUCAS,
M. J. O’DOHERTY,
patients who were assessed after treatment of the primary
tumour, 23 (38.3%) developed a recurrence locally or at a
distant site. There were nine (39.1%) isolated local recurrences and five (21.7%) isolated lung metastases. Eight
patients (34.7%) had lung metastases combined with other
sites of recurrence and one (4.3%) had isolated distant
metastases at sites other than the lung. Not all these patients
had FDG PET to identify these metastases.
There were 15 examples of local recurrence in 14
patients, one of whom developed a second recurrence. Of
the primary tumours 12 were high grade and two were
intermediate. Only three had a maximum diameter of less
than 5 cm. All local recurrences had had a marginal excision of the primary tumour, and 12 of these had been
performed at other hospitals. There were three recurrences
in two patients who were treated primarily in our centre.
Both had high-grade tumours; one was in the groin and the
other around the knee and they had had marginal excision
and postoperative radiotherapy.
Surgery for recurrence of STS, both locally and at distant
sites, is known to improve survival and decrease morbid3,6,7,28-35
The early detection of recurrence is therefore
ity.
advantageous and the use of a technique for whole-body
single scanning which is able to identify both local and
distant sites of recurrence is attractive.
There were five false-negative results, and three of these
patients subsequently developed positive MRI and FDG
PET scans within six months. A tumour was probably
present at the time of the initial FDG PET scan but in such
a small volume as to be undetectable. There is a limit to the
sensitivity of current techniques in detecting small volumes
of viable tumour and that of FDG PET may depend on the
grade of the tumour, reflecting the increased rate of glucose
36,37
metabolism in high-grade malignancies.
FDG PET
identified subclinical recurrences in four patients who had
previously had excision of high-grade sarcomas.
The three false-positive FDG PET scans can be
explained by the presence of inflammatory changes which
were confirmed on histological examination. Such a reactive response may continue for some time after operation
and must be taken into account when assessing individual
FDG PET scans. It is possible that the addition of local
transmission/emission scans of the area resected may give
quantitative data which will allow a tumour to be distinguished from an inflammatory change with more confidence. Our study considered only whole-body emission
scans since this allowed a standard throughput of patients at
a reasonable speed of scanning.
FDG PET was inferior to CT of the chest in detecting
lung metastases, failing to identify multiple deposits in two
cases. Both were high-grade tumours, one an extraskeletal
osteosarcoma and the other a leiomyosarcoma. In one, four
pulmonary metastases were present ranging from 16 to
43 mm in diameter and in the other there were seven
lesions ranging from 5 to 9 mm. FDG PET satisfactorily
identified the presence of lung metastases in four other
J. C. H. WONG,
ET AL
leiomyosarcomas and one extraskeletal osteosarcoma, the
size and location of the parenchymal metastases being
comparable.
One explanation for the failure of the FDG PET to
identify these lung metastases is that it may have been
taken too soon after injection of FDG. Scanning of the
chest was at between 45 and 90 minutes after injection, but
there is increasing evidence that maximum accumulation of
FDG in tumours is at about two hours after the injec38,39
tion;
the time which we allowed for the accumulation
of FDG in the metastases may have been insufficient to
allow their proper differentiation. Detection of lung metastases was based on the evaluation of whole-body FDG PET,
and lesions may be missed because of soft-tissue photon
attenuation by the chest. The addition of a localised transmission/emission scan may improve the contrast and
detectability of the metastases. Another reason for failure
may be that lung metastases do not have as good a vascular
supply as the original tumour until they reach a specific size
and this may restrict the uptake of FDG. This seems
unlikely in a richly vascular area such as the lung, but could
be investigated further using flow tracers.
FDG PET identified 13 other sites of metastases, only
five of which were clinically evident. One of these patients
had an epithelioid angiosarcoma located just above the
ankle. A below-knee amputation was performed for residual tumour after an incomplete primary excision at another
hospital. At the same time, a small lymph node in the
ipsilateral groin which had been identified as the site of a
metastasis on FDG PET, was removed; histological examination confirmed the diagnosis. The patient subsequently
developed two subclinical deposits in the thigh above the
amputation. Both were 0.5 cm in diameter and were identified by FDG PET. After excision of the latest metastasis,
the patient is free from disease 4 years and 5 months after
the original diagnosis.
MRI is the investigation of choice for recurrent and/or
residual local disease after operation for STS. CT is the
preferred investigation for pulmonary metastases. The differentiation between a recurrence and postoperative inflammatory change is difficult, and FDG PET can be useful in
helping to identify tumours, particularly those of high
grade, and is important in detecting metastatic spread at
other sites.
We found that FDG PET is not as satisfactory as conventional imaging for the identification of local recurrence
(MRI is better) and lung metastases (CT is better) in
patients with surgically-excised STS. It is, however, of
considerable value in detecting extrapulmonary visceral
spread. We believe that whole-body FDG PET has a major
role in the staging of STS both initially and at follow-up.
Whole-body scanning with specific views of the primary
tumour will allow quantitative measurement of the rate of
FDG metabolism. This, combined with the optimal timing
of scanning after injection of FDG, may greatly enhance
the sensitivity of this technique for the identification of
THE JOURNAL OF BONE AND JOINT SURGERY
FLUORODEOXYGLUCOSE POSITRON EMISSION TOMOGRAPHY IN SOFT-TISSUE SARCOMAS
both local and distant recurrence as a one-step procedure. A
combined approach utilising FDG PET with MRI and CT
will allow accurate assessment before treatment and aid the
monitoring of the effectiveness of subsequent treatment.
We wish to thank Mr H. D. Apthorp, Specialist Registrar in Orthopaedics,
St Thomas’ Hospital, London, UK, the South Thames NHS Executive
Research and Development Directorate (Ref: SPGS 431) and the Wishbone Trust, British Orthopaedic Association for their support.
No benefits in any form have been received or will be received from a
commercial party related directly or indirectly to the subject of this
article.
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